Studying the oxidation of water to molecular oxygen in photosynthetic and artificial systems by time-resolved membrane-inlet mass spectrometry

Shevela, Dmitriy; Messinger, Johannes

doi:10.3389/fpls.2013.00473

Cited by 32 publications

(28 citation statements)

References 72 publications

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“…This method, in which the gas molecules contained in the sample enter the vacuum of the mass spectrometer via pervaporation through a gaspermeable membrane, is therefore ideally suited to test the effect and mechanism of HCO − 3 interaction with PSII (23,24). The TR-MIMS experiments presented below were performed either in on-line or off-line mode.…”

Section: Resultsmentioning

confidence: 99%

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Koroidov

Shevela

Shutova

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Cyanobacteria, algae, and plants oxidize water to the O 2 we breathe, and consume CO 2 during the synthesis of biomass. Although these vital processes are functionally and structurally well separated in photosynthetic organisms, there is a long-debated role for CO 2 /HCO − 3 in water oxidation. Using membrane-inlet mass spectrometry we demonstrate that HCO − 3 acts as a mobile proton acceptor that helps to transport the protons produced inside of photosystem II by water oxidation out into the chloroplast's lumen, resulting in a light-driven production of O 2 and CO 2 . Depletion of HCO − 3 from the media leads, in the absence of added buffers, to a reversible down-regulation of O 2 production by about 20%. These findings add a previously unidentified component to the regulatory network of oxygenic photosynthesis and conclude the more than 50-y-long quest for the function of CO 2 / HCO − 3 in photosynthetic water oxidation.O xygenic photosynthesis in cyanobacteria, algae, and higher plants leads to the reduction of atmospheric CO 2 to energy-rich carbohydrates. The electrons needed for this process are extracted in a cyclic, light-driven process from water that is split into dioxygen (O 2 ) and protons. This reaction is catalyzed by a penta-μ-oxo bridged tetra-manganese calcium cluster (Mn 4 CaO 5 ) within the oxygen-evolving complex (OEC) of photosystem II (PSII) (1-4). The possible roles of inorganic carbon, C i ðC i = CO 2 ; H 2 CO 3 ; HCO − 3 ; CO 2− 3 Þ, in this process have been a controversial issue ever since Otto Warburg and Günter Krippahl (5) reported in 1958 that oxygen evolution by PSII strictly depends on CO 2 and therefore has to be based on the photolysis of H 2 CO 3 ("Kohlensäure") and not of water. These first experiments were indirect and, as became apparent later, were wrongly interpreted (6-8). Several research groups followed up on these initial results and identified two possible sites of C i interaction within PSII (reviewed in refs. 9-12). Functional and spectroscopic studies showed that HCO − 3 facilitates the reduction of the secondary plastoquinone electron acceptor (Q B ) of PSII by participating in the protonation of Q 2− B . Binding of HCO − 3 (or CO 2− 3 ) to the nonheme Fe between the quinones Q A and Q B was recently confirmed by X-ray crystallography (3,13,14). Despite this functional role at the acceptor side, the very tight binding of HCO − 3 to this site makes it impossible for the activity of PSII to be affected by changing the C i level of the medium; instead inhibitors such as formate need to be added to induce the acceptor-side effect (15). Consequently, the watersplitting electron-donor side of PSII has also been studied intensively (for recent reviews, see refs. 11 and 12). Although a tight binding of C i near the Mn 4 CaO 5 cluster is excluded on the basis of X-ray crystallography (3, 14), FTIR spectroscopy (16), and mass spectrometry (17, 18), the possibility that a weakly bound HCO − 3 affects the activity of PSII at the donor side remains a viable option (reviewed i...

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Section: Resultsmentioning

confidence: 99%

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Koroidov

Shevela

Shutova

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…[105] CO 2 was also measured simultaneously to determine the corrosion of the carbon supports. For this, ag as-tight electrochemical cell was assembled, which contained the working and reference electrodes in the main compartment and the counter electrode in as econd compartment.…”

Section: Electrochemistrymentioning

confidence: 99%

Electrocatalytic Water Oxidation by MnO_x/C: In Situ Catalyst Formation, Carbon Substrate Variations, and Direct O₂/CO₂ Monitoring by Membrane‐Inlet Mass Spectrometry

et al. 2017

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Layers of amorphous manganese oxides were directly formed on the surfaces of different carbon materials by exposing the carbon to aqueous solutions of permanganate (MnO4−) followed by sintering at 100–400 °C. During electrochemical measurements in neutral aqueous buffer, nearly all of the MnOx/C electrodes show significant oxidation currents at potentials relevant for the oxygen evolution reaction (OER). However, by combining electrolysis with product detection by using mass spectrometry, it was found that these currents were only strictly linked to water oxidation if MnOx was deposited on graphitic carbon materials (faradaic O2 yields >90 %). On the contrary, supports containing sp3‐C were found to be unsuitable as the OER is accompanied by carbon corrosion to CO2. Thus, choosing the “right” carbon material is crucial for the preparation of stable and efficient MnOx/C anodes for water oxidation catalysis. For MnOx on graphitic substrates, current densities of >1 mA cm−2 at η=540 mV could be maintained for at least 16 h of continuous operation at pH 7 (very good values for electrodes containing only abundant elements such as C, O, and Mn) and post‐operando measurements proved the integrity of both the catalyst coating and the underlying carbon at OER conditions.

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“…This type of mass spectrometer is normally equipped with an electron-impact ion source, magnetic sector field analyser, and individual detectors (Faraday cups) that provide simultaneous detection of several masses (ions) with high sensitivity and signal stability. For its ability to monitor and to selectively analyze all isotopologues (molecules that differ only in their isotopic composition) of gaseous products with one instrument, the TR-MIMS approach in combination with isotope enrichments became an indispensable tool for kinetic and functional analyses of photosynthetic enzymes [71–73]. The key part of the TR-MIMS instrument is a gas inlet system that is integrated within a MIMS cell.…”

Section: Membrane Inlet Mass Spectrometry and Photosystem IImentioning

confidence: 99%

Light-Dependent Production of Dioxygen in Photosynthesis

Yano

Kern

Yachandra

et al. 2014

Metal Ions in Life Sciences

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Oxygen, that supports all aerobic life, is abundant in the atmosphere because of its constant regeneration by photosynthetic water oxidation, which is catalyzed by a Mn4CaO5 cluster in photosystem II (PS II), a multi subunit membrane protein complex. X-ray and other spectroscopy studies of the electronic and geometric structure of the Mn4CaO5 cluster as it advances through the inter-mediate states have been important for understanding the mechanism of water oxidation. The results and interpretations, especially from X-ray spectroscopy studies, regarding the geometric and electronic structure and the changes as the system proceeds through the catalytic cycle will be summarized in this review. This review will also include newer methodologies in time-resolved X-ray diffraction and spectroscopy that have become available since the commissioning of the X-ray free electron laser (XFEL) and are being applied to study the oxygen-evolving complex (OEC). The femtosecond X-ray pulses of the XFEL allows us to outrun X-ray damage at room temperature, and the time-evolution of the photo-induced reaction can be probed using a visible laser-pump followed by the X-ray-probe pulse. XFELs can be used to simultaneously determine the light-induced protein dynamics using crystallography and the local chemistry that occurs at the catalytic center using X-ray spectroscopy under functional conditions. Membrane inlet mass spectrometry has been important for providing direct information about the exchange of substrate water molecules, which has a direct bearing on the mechanism of water oxidation. Moreover, it has been indispensable for the time-resolved X-ray diffraction and spectroscopy studies and will be briefly reviewed in this chapter. Given the role of PS II in maintaining life in the biosphere and the future vision of a renewable energy economy, understanding the structure and mechanism of the photosynthetic water oxidation catalyst is an important goal for the future.

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Studying the oxidation of water to molecular oxygen in photosynthetic and artificial systems by time-resolved membrane-inlet mass spectrometry

Cited by 32 publications

References 72 publications

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Electrocatalytic Water Oxidation by MnO_x/C: In Situ Catalyst Formation, Carbon Substrate Variations, and Direct O₂/CO₂ Monitoring by Membrane‐Inlet Mass Spectrometry

Light-Dependent Production of Dioxygen in Photosynthesis

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Studying the oxidation of water to molecular oxygen in photosynthetic and artificial systems by time-resolved membrane-inlet mass spectrometry

Cited by 32 publications

References 72 publications

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Electrocatalytic Water Oxidation by MnOx/C: In Situ Catalyst Formation, Carbon Substrate Variations, and Direct O2/CO2 Monitoring by Membrane‐Inlet Mass Spectrometry

Light-Dependent Production of Dioxygen in Photosynthesis

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Electrocatalytic Water Oxidation by MnO_x/C: In Situ Catalyst Formation, Carbon Substrate Variations, and Direct O₂/CO₂ Monitoring by Membrane‐Inlet Mass Spectrometry